Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids

Jiankai Wei; Wei Zhang; An Jiang; Hongzhe Peng; Quanyong Zhang; Yuting Li; Jianqing Bi; Linting Wang; Penghui Liu; Jing Wang; Yonghang Ge; Liya Zhang; Haiyan Yu; Lei Li; Shi Wang; Liang Leng; Kai Chen; Bo Dong

doi:10.1038/s41467-024-46780-0

Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids

Nat Commun. 2024 Mar 16;15(1):2395. doi: 10.1038/s41467-024-46780-0.

Authors

Jiankai Wei^#^{1

2

3}, Wei Zhang^#¹, An Jiang^#¹, Hongzhe Peng^#¹, Quanyong Zhang^#⁴, Yuting Li¹, Jianqing Bi¹, Linting Wang⁵, Penghui Liu¹, Jing Wang¹, Yonghang Ge¹, Liya Zhang⁴, Haiyan Yu¹, Lei Li⁵, Shi Wang^{1

2}, Liang Leng⁶, Kai Chen^{7

8}, Bo Dong^{9

10

11}

Affiliations

¹ Fang Zongxi Center for Marine EvoDevo, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.
² Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, 266237, China.
³ MoE Key Laboratory of Evolution and Marine Biodiversity, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003, China.
⁴ State Key Laboratory of Primate Biomedical Research and Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, 650500, China.
⁵ National Center of Mathematics and Interdisciplinary Sciences, Academy of Mathematics and Systems Science, Chinese Academy of Sciences, Beijing, 100190, China.
⁶ Institute of Herbgenomics, Chengdu University of Traditional Chinese Medicine, Chengdu, 611137, China. lleng@icmm.ac.cn.
⁷ State Key Laboratory of Primate Biomedical Research and Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, 650500, China. chen_kai@gmlab.ac.cn.
⁸ Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), No. 1119 Haibin Rd, Nansha Dist., Guangzhou, 511458, China. chen_kai@gmlab.ac.cn.
⁹ Fang Zongxi Center for Marine EvoDevo, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China. bodong@ouc.edu.cn.
¹⁰ Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, 266237, China. bodong@ouc.edu.cn.
¹¹ MoE Key Laboratory of Evolution and Marine Biodiversity, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003, China. bodong@ouc.edu.cn.

^# Contributed equally.

Abstract

Zygotic genome activation (ZGA) is a universal process in early embryogenesis of metazoan, when the quiescent zygotic nucleus initiates global transcription. However, the mechanisms related to massive genome activation and allele-specific expression (ASE) remain not well understood. Here, we develop hybrids from two deeply diverged (120 Mya) ascidian species to symmetrically document the dynamics of ZGA. We identify two coordinated ZGA waves represent early developmental and housekeeping gene reactivation, respectively. Single-cell RNA sequencing reveals that the major expression wave exhibits spatial heterogeneity and significantly correlates with cell fate. Moreover, allele-specific expression occurs in a species- rather than parent-related manner, demonstrating the divergence of cis-regulatory elements between the two species. These findings provide insights into ZGA in chordates.

MeSH terms

Alleles
Animals
Chordata*
Embryonic Development / genetics
Gene Expression Regulation, Developmental
Urochordata* / genetics
Zygote / metabolism